Nile tilapia TRIM39 recruits I3K413 and I3KL45 as adaptors and is involved in the NF-κB pathway.


Journal

Journal of fish biology
ISSN: 1095-8649
Titre abrégé: J Fish Biol
Pays: England
ID NLM: 0214055

Informations de publication

Date de publication:
Jul 2022
Historique:
received: 31 03 2022
accepted: 29 04 2022
pubmed: 7 5 2022
medline: 22 7 2022
entrez: 6 5 2022
Statut: ppublish

Résumé

Tripartite motif (TRIM) proteins play a regulatory function in cancer, cell apoptosis and innate immunity. To understand the role of TRIM39 in Nile tilapia (Oreochromis niloticus), TRIM39 cDNA was isolated. The total length of TRIM39 cDNA was 5025 bp. The deduced OnTRIM39 protein contains 549 amino acids and has conserved domains of the TRIM family, which are the RING, B-box, coiled-coil and PRY-SPRY domains. OnTRIM39 mRNA was widely expressed in various tissues. After challenge with Streptococcus agalactiae and stimulation with polyinosinic polycytidylic acid [poly (I:C)] and lipopolysaccharides (LPS), the amount of OnTRIM39 transcript was changed in various tested tissues. OnTRIM39 overexpression increased NF-κB activity. OnTRIM39 was present in the cytoplasm. Mass spectrometry of proteins pulled down with recombinant OnTRIM39 showed that 250 proteins potentially interact with OnTRIM39. The authors selected I3K4I3 from the 250 candidate proteins to verify its interaction with TRIM39. They also selected I3KL45, a member of the same 14-3-3 protein family, to verify its interaction with TRIM39. The results of pull-down assays showed that OnTRIM39 interacted with both I3K413 and I3KL45. These results contribute to further study of the innate immune mechanism of tilapia.

Identifiants

pubmed: 35514248
doi: 10.1111/jfb.15079
doi:

Substances chimiques

DNA, Complementary 0
Fish Proteins 0
NF-kappa B 0
Ubiquitin-Protein Ligases EC 2.3.2.27
Poly I-C O84C90HH2L

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

144-153

Informations de copyright

© 2022 Fisheries Society of the British Isles.

Références

Ao, J., Mu, Y., Wang, K., Sun, M., Wang, X., & Chen, X. (2016). Identification and characterization of a novel toll-like receptor 2 homologue in the large yellow croaker Larimichthys crocea. Fish & Shellfish Immunology, 48, 221-227.
Boudinot, P., van der Aa, L. M., Jouneau, L., Du Pasquier, L., Pontarotti, P., Briolat, V., … Levraud, J. P. (2011). Origin and evolution of TRIM proteins: New insights from the complete TRIM repertoire of zebrafish and pufferfish. PLoS One, 6, 18.
Cammas, F., Khetchoumian, K., Chambon, P., & Losson, R. (2012). TRIM involvement in transcriptional regulation. Oxygen Transport to Tissue XXXIII, 770, 59-76.
Chan, Y. K., & Gack, M. U. (2016). Small molecules that target phosphorylation dependent protein-protein interaction. Nature Immunology, 17(5), 523-530.
Chen, B., Huo, S., Liu, W., Wang, F., Lu, Y., Xu, Z., & Liu, X. (2019). Fish-specific finTRIM FTR36 triggers IFN pathway and mediates inhibition of viral replication. Fish and Shellfish Immunology, 84, 876-884.
Chen, Z., Wang, Z., Guo, W., Zhang, Z., Zhao, F., Zhao, Y., … He, X. (2015). TRIM35 interacts with pyruvate kinase isoform M2 to suppress the Warburg effect and tumorigenicity in hepatocellular carcinoma. Oncogene, 34, 3946-3956.
Claudio, A. P., Joazeiro, C. A., & Weissman, A. M. (2000). RING finger proteins: Mediators of ubiquitin ligase activity. Cell, 102, 549-552.
dos Santos, C. C., Han, B., Andrade, C. F., Bai, X., Uhlig, S., Hubmayr, R., … Liu, M. (2004). DNA microarray analysis of gene expression in alveolar epithelial cells in response to TNFalpha, LPS, and cyclic stretch. Physiological Genomics, 19, 331-342.
Freemont, P. (2000). Ubiquitination: RING for destruction? Current Biology: CB, 10, R84-R87.
Funami, K., Matsumoto, M., Obuse, C., & Seya, T. (2016). 14-3-3-zeta participates in TLR3-mediated TICAM-1 signal-platform formation. Molecular Immunology, 73, 60-68.
Gack, M. U., Shin, Y. C., Joo, C.-H., Urano, T., Liang, C., Sun, L., … Jung, J. U. (2007). TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature, 446, 916-920.
Gao, F. Y., Liu, J., Lu, M. X., Liu, Z. G., Wang, M., Ke, X. L., … Cao, J. M. (2021b). Nile tilapia toll-like receptor 7 subfamily: Intracellular TLRs that recruit MyD88 as an adaptor and activate the NF-κB pathway in the immune response. Developmental & Comparative Immunology, 125(125), 104173.
Gao, F. Y., Pang, J. C., Wang, M., Lu, M. X., Liu, Z. G., Cao, J. M., … Yi, M. M. (2021a). Structurally diverse genes encode TLR13 in Nile tilapia: The two receptors can recognize streptococcus 23S RNA and conduct signal transduction through MyD88. Molecular Immunology, 132, 60-78.
Gao, F. Y., Zhou, X., Lu, M. X., Wang, M., Liu, Z. G., Cao, J. M., … Qiu, D. G. (2022). TLR1 in Nile tilapia: The conserved receptor cannot interact with MyD88 and TIRAP but can activate NF-κB in vitro. Developmental & Comparative Immunology, 127, 104300.
van Gent, M., Sparrer, K. M. J., & Gack, M. U. (2018). TRIM proteins and their roles in antiviral host defenses. Annual Review of Virology, 5, 385-405.
Grutter, C., Briand, C., Capitani, G., Mittl, P. R., Papin, S., Tschopp, J., & Grutter, M. G. (2006). Structure of the PRYSPRY-domain: Implications for autoinflammatory diseases. FEBS Letters, 580, 99-106.
Hatakeyama, S. (2011). TRIM proteins and cancer. Nature Reviews Cancer, 11, 792-804.
Huang, Y., Zhang, J., Liu, J., Hu, Y., Ni, S., Yang, Y., … Qin, Q. (2017). Fish TRIM35 negatively regulates the interferon signaling pathway in response to grouper nodavirus infection. Fish and Shellfish Immunology, 69, 142-152.
Ichimura, T., Isobe, T., Okuyama, T., Fau, N. O. T., Takahashi, K., Fau, T. N., … Takahashi, Y. (1988). Molecular cloning of cDNA coding for brain-specific 14-3-3 protein. National Academy of Sciences of U.S.A, 85, 7084-7088.
Ikeda, K., & Inoue, S. (2012). Trim proteins as ring finger E3 ubiquitin ligases. Advances in Experimental Medicine and Biology, 770, 27-37.
Kawai, T., & Akira, S. (2011). Regulation of innate immune signalling pathways by the tripartite motif (TRIM) family proteins. EMBO Molecular Medicine, 3, 513-527.
Kimura, F., Suzu, S., Nakamura, Y., Nakata, Y., Yamada, M., Kuwada, N., … Motoyoshi, K. (2003). Cloning and characterization of a novel RING-B-box-coiled-coil protein with apoptotic function. The Journal of Biological Chemistry, 278, 25046-25054.
Koepke, L., Gack, M. U., & Sparrer, K. M. (2021). The antiviral activities of TRIM proteins. Current Opinion in Microbiology, 59, 50-57.
Kurata, R., Tajima, A., Yonezawa, T., & Inoko, H. (2013). TRIM39R, but not TRIM39B, regulates type I interferon response. Biochemical and Biophysical Research Communications, 436, 90-95.
Langevin, C., Aleksejeva, E., Houel, A., Briolat, V., Torhy, C., Lunazzi, A., … Boudinot, P. (2017). FTR83, a member of the large fish-specific finTRIM family, triggers IFN pathway and counters viral infection. Frontiers in Immunology, 8, 617.
Langevin, C., Levraud, J. P., & Boudinot, P. (2019). Fish antiviral tripartite motif (TRIM) proteins. Fish and Shellfish Immunology, 86, 724-733.
Li, X., Kim, J., Song, B., Finzi, A., Pacheco, B., & Sodroski, J. (2013). Virus-specific effects of TRIM5α(rh) RING domain functions on restriction of retroviruses. Journal of Virology, 87, 7234-7245.
Liu, H. M., Loo, Y. M., Horner, S. M., Zornetzer, G. A., Katze, M. G., & Gale, M., Jr. (2012). The mitochondrial targeting chaperone 14-3-3epsilon regulates a RIG-I translocon that mediates membrane association and innate antiviral immunity. Cell Host & Microbe, 11, 528-537.
Martin-Vicente, M., Medrano, L. M., Resino, S., Garcia-Sastre, A., & Martinez, I. (2017). TRIM25 in the regulation of the antiviral innate immunity. Frontiers in Immunology, 8, 1187.
Massiah, M. A., Simmons, B. N., Short, K. M., & Cox, T. C. (2006). Solution structure of the RBCC/TRIM B-box1 domain of human MID1: B-box with a RING. Journal of Molecular Biology, 358, 532-545.
Meroni, G., & Diez-Roux, G. (2005). TRIM/RBCC, a novel class of ‘single protein RING finger’ E3 ubiquitin ligases. BioEssays, 27, 1147-1157.
Muslin, A. J., Tanner, J. W., Allen, P. M., & Shaw, A. S. (1996). Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell, 84, 889-897.
Ozato, K., Shin, D. M., Chang, T. H., & Morse, H. C. (2008). TRIM family proteins and their emerging roles in innate immunity. Nature Reviews Immunology, 8, 849-860.
Pang, J. C., Gao, F. Y., Lu, M. X., Ye, X., Zhu, H. P., & Ke, X. L. (2013). Major histocompatibility complex class IIA and IIB genes of Nile tilapia Oreochromis niloticus: Genomic structure, molecular polymorphism and expression patterns. Fish and Shellfish Immunology, 34, 486-496.
Rajsbaum, R., Garcia-Sastre, A., & Versteeg, G. A. (2014). TRIMmunity: The roles of the TRIM E3-ubiquitin ligase family in innate antiviral immunity. Journal of Molecular Biology, 426, 1265-1284.
Sanchez, J. G., Chiang, J. J., Sparrer, K. M. J., Alam, S. L., Chi, M., Roganowicz, M. D., … Pornillos, O. (2016). Mechanism of TRIM25 catalytic activation in the antiviral RIG-I pathway. Cell Reports, 16, 1315-1325.
Schwamborn, J., Lindecke, A., Elvers, M., Horejschi, V., Kerick, M., Rafigh, M., … Kaltschmidt, C. (2003). Microarray analysis of tumor necrosis factor α induced gene expression in U373 human glioblastoma cells. BMC Genomics, 4, 46.
Shi, Y., Hu, S., Duan, W., Ding, T., & Zhao, Z. (2019). The distinct evolutionary properties of the tripartite motif-containing protein 39 in the Chinese softshell turtle based on its structural and functional characterization. Developmental and Comparative Immunology, 99, 103407.
Sun, N., Jiang, L., Ye, M., Wang, Y., Wang, G., Wan, X., … Li, C. (2020). TRIM35 mediates protection against influenza infection by activating TRAF3 and degrading viral PB2. Protein. Cell, 11, 894-914.
Suzuki, M., Watanabe, M., Nakamaru, Y., Takagi, D., Takahashi, H., Fukuda, S., & Hatakeyama, S. (2016). TRIM39 negatively regulates the NFkappaB-mediated signaling pathway through stabilization of Cactin. Cellular and Molecular Life Sciences, 73, 1085-1101.
Wang, W., Huang, Y., Yu, Y., Yang, Y., Xu, M., Chen, X., … Huang, X. (2016). Fish TRIM39 regulates cell cycle progression and exerts its antiviral function against iridovirus and nodavirus. Fish and Shellfish Immunology, 50, 1-10.
Wang, Y., Yan, S., Yang, B., Wang, Y., Zhou, H., Lian, Q., & Sun, B. (2015). TRIM35 negatively regulates TLR7- and TLR9-mediated type I interferon production by targeting IRF7. FEBS Letters, 589, 1322-1330.
Wu, M., Dan, C., Gui, J. F., & Zhang, Y. B. (2019). Fish species-specific TRIM gene FTRCA1 negatively regulates interferon response through attenuating IRF7 transcription. Fish and Shellfish Immunology, 90, 180-187.
Yergeau, D. A., Cornell, C. N., Parker, S. K., Zhou, Y., & Detrich, H. W. (2005). Bloodthirsty, an RBCC/TRIM gene required for erythropoiesis in zebrafish. Developmental Biology, 283, 97-112.
Zhang, H. H., & Zhang, L. (2018). Research progress of TRIM in the innate immune signaling pathway. Journal of Biology, 35, 77-80.
Zhang, X., Zhao, H., Chen, Y., Luo, H., Yang, P., & Yao, B. (2015). A zebrafish (Danio rerio) bloodthirsty member 20 with E3 ubiquitin ligase activity involved in immune response against bacterial infection. Biochemical and Biophysical Research Communications, 457, 83-89.
Zhao, W., Wang, L., Zhang, M., Yuan, C., & Gao, C. (2012). E3 ubiquitin ligase tripartite motif 38 negatively regulates TLR-mediated immune responses by proteasomal degradation of TNF receptor-associated factor 6 in macrophages. Journal of Immunology, 188, 2567-2574.
Zhou, X., Gao, F. Y., Lu, M. X., Liu, Z. G., Wang, M., Cao, J. M., … Yi, M. M. (2022). DDX43 recruits TRIF or IPS-1 as an adaptor and activates the IFN-β pathway in Nile tilapia (Oreochromis niloticus). Molecular Immunology, 143, 7-16.

Auteurs

Feng-Ying Gao (FY)

Key Laboratory of Tropical & Subtropical Fishery Resource Application & Cultivation, Ministry of Agriculture/Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou, China.
Maoming Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Maoming, China.

Xin Zhou (X)

College of Fisheries and Life Science, Shanghai Ocean University, Shanghai, China.

Mai-Xin Lu (MX)

Key Laboratory of Tropical & Subtropical Fishery Resource Application & Cultivation, Ministry of Agriculture/Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou, China.
Maoming Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Maoming, China.

Miao Wang (M)

Key Laboratory of Tropical & Subtropical Fishery Resource Application & Cultivation, Ministry of Agriculture/Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou, China.
Maoming Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Maoming, China.

Zhi-Gang Liu (ZG)

Key Laboratory of Tropical & Subtropical Fishery Resource Application & Cultivation, Ministry of Agriculture/Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou, China.
Maoming Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Maoming, China.

Jiang-Meng Cao (JM)

Key Laboratory of Tropical & Subtropical Fishery Resource Application & Cultivation, Ministry of Agriculture/Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou, China.
Maoming Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Maoming, China.

Xiao-Li Ke (XL)

Key Laboratory of Tropical & Subtropical Fishery Resource Application & Cultivation, Ministry of Agriculture/Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou, China.
Maoming Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Maoming, China.

Meng-Meng Yi (MM)

Key Laboratory of Tropical & Subtropical Fishery Resource Application & Cultivation, Ministry of Agriculture/Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou, China.
Maoming Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Maoming, China.

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